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Rice Protocols pp 269-283 | Cite as

Molecular Approaches to Improve Rice Abiotic Stress Tolerance

Protocol
First Online:
Part of the Methods in Molecular Biology book series (MIMB, volume 956)

Abstract

Abiotic stress is a major factor limiting productivity of rice crops in large areas of the world. Because plants cannot avoid abiotic stress by moving, they have acquired various mechanisms for stress tolerance in the course of their evolution. Enhancing or introducing such mechanisms in rice is one effective way to develop stress-tolerant cultivars. Based on physiological studies on stress responses, recent progress in plant molecular biology has enabled discovery of many genes involved in stress tolerance. These genes include regulatory genes, which regulate stress response (e.g., transcription factors and protein kinases), and functional genes, which protect the cell (e.g., enzymes for generating protective metabolites and proteins). Both kinds of genes are used to increase stress tolerance in rice. In addition, several quantitative trait loci (QTLs) associated with higher stress tolerance have been cloned, contributing to the discovery of significantly important genes for stress tolerance.

Key words

Abiotic stress Stress tolerance Transgenic rice Transcription factor Protein kinase Metabolic engineering Stress-inducible promoter 
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References

  1. 1.
    Riechmann JL, Heard J, Martin G et al (2000) Arabidopsis transcription factors: genome-wide comparative analysis among eukaryotes. Science 290:2105–2110PubMedCrossRefGoogle Scholar
  2. 2.
    Goff SA, Ricke D, Lan T-H et al (2002) A draft sequence of the rice genome (Oryza sativa L. Ssp. japonica). Science 296:92–100PubMedCrossRefGoogle Scholar
  3. 3.
    Shiu S-H, Shih M-C, Li W-H (2005) Transcription factor families have much higher expansion rates in plants than in animals. Plant Physiol 139:18–26PubMedCrossRefGoogle Scholar
  4. 4.
    Alonso-Blanco C, Gomez-Mena C, Llorente F, Koornneef M, Salinas J, Martínez-Zapater JM (2005) Genetic and molecular analyses of natural variation indicate CBF2 as a candidate gene for underlying a freezing tolerance quantitative trait locus in Arabidopsis. Plant Physiol 139:1304–1312PubMedCrossRefGoogle Scholar
  5. 5.
    Francia E, Barabaschi D, Tondelli A et al (2007) Fine mapping of a hv CBF gene cluster at the frost resistance locus Fr-H2 in barley. Theor Appl Genet 115:1083–1091PubMedCrossRefGoogle Scholar
  6. 6.
    Vágújfalvi A, Galiba G, Cattivelli L, Dubcovsky J (2003) The cold-regulated transcriptional activator Cbf3 is linked to the frost-tolerance locus Fr-A2 on wheat chromosome 5A. Mol Gen Genomics 269:60–67Google Scholar
  7. 7.
    Knox AK, Li C, Vágújfalvi A, Galiba G, Stockinger EJ, Dubcovsky J (2008) Identification of candidate CBF genes for the frost tolerance locus Fr-A m 2 in Triticum monococcum. Plant Mol Biol 67:257–270PubMedCrossRefGoogle Scholar
  8. 8.
    Fukao T, Xu K, Ronald PC, Bailey-Serres J (2006) A variable cluster of ethylene response factor-like genes regulates metabolic and developmental acclimation responses to submergence in rice. Plant Cell 18:2021–2034PubMedCrossRefGoogle Scholar
  9. 9.
    Xu K, Xu X, Fukao T et al (2006) Sub1A is an ethylene-response-factor-like gene that confers submergence tolerance to rice. Nature 442:705–708PubMedCrossRefGoogle Scholar
  10. 10.
    Jaglo-Ottosen KR, Gilmour SJ, Zarka DG, Schabenberger O, Thomashow MF (1998) Arabidopsis CBF1 overexpression induces COR genes and enhances freezing tolerance. Science 280:104–106PubMedCrossRefGoogle Scholar
  11. 11.
    Liu Q, Kasuga M, Sakuma Y et al (1998) Two transcription factors, DREB1 and DREB2, with an EREBP/AP2 DNA binding domain separate two cellular signal transduction pathways in drought- and low-temperature-responsive gene expression, respectively, in Arabidopsis. Plant Cell 10:1391–1406PubMedGoogle Scholar
  12. 12.
    Sakuma Y, Maruyama K, Qin F, Osakabe Y, Shinozaki K, Yamaguchi-Shinozaki K (2006) Dual function of an Arabidopsis transcription factor DREB2A in water-stress-responsive and heat-stress-responsive gene expression. Proc Natl Acad Sci USA 103:18822–18827PubMedCrossRefGoogle Scholar
  13. 13.
    Kasuga M, Liu Q, Miura S, Yamaguchi-Shinozaki K, Shinozaki K (1999) Improving plant drought, salt, and freezing tolerance by gene transfer of a single stress-inducible transcription factor. Nat Biotechnol 17:287–291PubMedCrossRefGoogle Scholar
  14. 14.
    Nakashima K, Ito Y, Yamaguchi-Shinozaki K (2009) Transcriptional regulatory networks in response to abiotic stresses in Arabidopsis and grasses. Plant Physiol 149:88–95PubMedCrossRefGoogle Scholar
  15. 15.
    Yamaguchi-Shinozaki K, Shinozaki K (2006) Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu Rev Plant Biol 57:781–803PubMedCrossRefGoogle Scholar
  16. 16.
    Ito Y, Katsura K, Maruyama K et al (2006) Functional analysis of rice DREB1/CBF-type transcription factors involved in cold-responsive gene expression in transgenic rice. Plant Cell Physiol 47:141–153PubMedCrossRefGoogle Scholar
  17. 17.
    Oh S-J, Song SI, Kim YS et al (2005) Arabidopsis CBF3/DREB1A and ABF3 in transgenic rice increased tolerance to abiotic stress without stunting growth. Plant Physiol 138:341–351PubMedCrossRefGoogle Scholar
  18. 18.
    Chen J-Q, Meng X-P, Zhang Y, Xia M, Wang X-P (2008) Over-expression of OsDREB genes lead to enhanced drought tolerance in rice. Biotechnol Lett 30:2191–2198PubMedCrossRefGoogle Scholar
  19. 19.
    Wang Q, Guan Y, Wu Y, Chen H, Chen F, Chu C (2008) Overexpression of a rice OsDREB1F gene increases salt, drought, and low temperature tolerance in both Arabidopsis and rice. Plant Mol Biol 67:589–602PubMedCrossRefGoogle Scholar
  20. 20.
    Oh S-J, Kwon C-W, Choi D-W, Song SI, Kim J-K (2007) Expression of barley HvCBF4 enhances tolerance to abiotic stress in transgenic rice. Plant Biotechnol J 5:646–656PubMedCrossRefGoogle Scholar
  21. 21.
    Qin F, Kakimoto M, Sakuma Y et al (2007) Regulation and functional analysis of ZmDREB2A in response to drought and heat stresses in Zea mays L. Plant J 50:54–69PubMedCrossRefGoogle Scholar
  22. 22.
    Qin F, Sakuma Y, Tran L-SP et al (2008) Arabidopsis DREB2A-interacting proteins function as RING E3 ligases and negatively regulate plant drought stress-responsive gene expression. Plant Cell 20:1693–1707PubMedCrossRefGoogle Scholar
  23. 23.
    Sakuma Y, Maruyama K, Osakabe Y et al (2006) Functional analysis of an Arabidopsis transcription factor, DREB2A, involved in drought-responsive gene expression. Plant Cell 18:1292–1309PubMedCrossRefGoogle Scholar
  24. 24.
    Karaba A, Dixit S, Greco R et al (2007) Improvement of water use efficiency in rice by expression of HARDY, an Arabidopsis drought and salt tolerance gene. Proc Natl Acad Sci USA 104:15270–15275PubMedCrossRefGoogle Scholar
  25. 25.
    Finkelstein RR, Gampala SSL, Rock CD (2002) Abscisic acid signaling in seeds and seedlings. Plant Cell 14:S15–S45PubMedGoogle Scholar
  26. 26.
    Rabbani MA, Maruyama K, Abe H et al (2003) Monitoring expression profiles of rice genes under cold, drought, and high-salinity stresses and abscisic acid application using cDNA microarray and RNA gel-blot analyses. Plant Physiol 133:1755–1767PubMedCrossRefGoogle Scholar
  27. 27.
    Hobo T, Kowyama Y, Hattori T (1999) A bZIP factor, TRAB1, interacts with VP1 and mediates abscisic acid-induced transcription. Proc Natl Acad Sci USA 96:15348–15353PubMedCrossRefGoogle Scholar
  28. 28.
    Choi H, Hong J, Ha J, Kang J, Kim SY (2000) ABFs, a family of ABA-responsive element binding factors. J Biol Chem 275:1723–1730PubMedCrossRefGoogle Scholar
  29. 29.
    Uno Y, Furihata T, Abe H, Yoshida R, Shinozaki K, Yamaguchi-Shinozaki K (2000) Arabidopsis basic leucine zipper transcription factors involved in an abscisic acid-dependent signal transduction pathway under drought and high-salinity conditions. Proc Natl Acad Sci USA 97:11632–11637PubMedCrossRefGoogle Scholar
  30. 30.
    Kagaya Y, Hobo T, Murata M, Ban A, Hattori T (2002) Abscisic acid-induced transcription is mediated by phosphorylation of an abscisic acid response element binding factor, TRAB1. Plant Cell 14:3177–3189PubMedCrossRefGoogle Scholar
  31. 31.
    Furihata T, Maruyama K, Fujita Y et al (2006) Abscisic acid-dependent multisite phosphorylation regulates the activity of a transcription activator AREB1. Proc Natl Acad Sci USA 103:1988–1993PubMedCrossRefGoogle Scholar
  32. 32.
    Kim S, Kang JY, Cho D-I, Park J-H, Kim SY (2004) ABF2, an ABRE-binding bZIP factor, is an essential component of glucose signaling and its overexpression affects multiple stress tolerance. Plant J 40:75–87PubMedCrossRefGoogle Scholar
  33. 33.
    Fujita Y, Fujita M, Satoh R et al (2005) AREB1 is a transcription activator of novel ABRE-dependent ABA signaling that enhances drought stress tolerance in Arabidopsis. Plant Cell 17:3470–3488PubMedCrossRefGoogle Scholar
  34. 34.
    Xiang Y, Tang N, Du H, Ye H, Xiong L (2008) Characterization of OsbZIP23 as a key player of the basic leucine zipper transcription factor family for conferring abscisic acid sensitivity and salinity and drought tolerance in rice. Plant Physiol 148:1938–1952PubMedCrossRefGoogle Scholar
  35. 35.
    Fujita M, Fujita Y, Maruyama K et al (2004) A dehydration-induced NAC protein, RD26, is involved in a novel ABA-dependent stress-signaling pathway. Plant J 39:863–876PubMedCrossRefGoogle Scholar
  36. 36.
    Tran L-SP, Nakashima K, Sakuma Y et al (2004) Isolation and functional analysis of Arabidopsis stress-inducible NAC transcription factors that bind to a drought-responsive cis-element in the early responsive to dehydration stress 1 promoter. Plant Cell 16:2481–2498PubMedCrossRefGoogle Scholar
  37. 37.
    Nakashima K, Tran L-SP, Van Nguyen D et al (2007) Functional analysis of a NAC-type transcription factor OsNAC6 involved in abiotic and biotic stress-responsive gene expression in rice. Plant J 51:617–630PubMedCrossRefGoogle Scholar
  38. 38.
    Hu H, Dai M, Yao J et al (2006) Overexpressing a NAM, ATAF, and CUC (NAC) transcription factor enhances drought resistance and salt tolerance in rice. Proc Natl Acad Sci USA 103:12987–12992PubMedCrossRefGoogle Scholar
  39. 39.
    Hu H, You J, Fang Y, Zhu X, Qi Z, Xiong L (2008) Characterization of transcription factor gene SNAC2 conferring cold and salt tolerance in rice. Plant Mol Biol 67:169–181PubMedCrossRefGoogle Scholar
  40. 40.
    Wu X, Shiroto Y, Kishitani S, Ito Y, Toriyama K (2009) Enhanced heat and drought tolerance in transgenic rice seedlings overexpressing OsWRKY11 under the control of HSP101 promoter. Plant Cell Rep 28:21–30PubMedCrossRefGoogle Scholar
  41. 41.
    Boudsocq M, Laurière C (2005) Osmotic signaling in plants. Multiple pathways mediated by emerging kinase families. Plant Physiol 138:1185–1194PubMedCrossRefGoogle Scholar
  42. 42.
    Kobayashi Y, Yamamoto S, Minami H, Kagaya Y, Hattori T (2004) Differential activation of the rice sucrose nonfermenting1-related protein kinase2 family by hyperosmotic stress and abscisic acid. Plant Cell 16:1163–1177PubMedCrossRefGoogle Scholar
  43. 43.
    Mustilli A-C, Merlot S, Vavasseur A, Fenzi F, Giraudat J (2002) Arabidopsis OST1 protein kinase mediates the regulation of stomatal aperture by abscisic acid and acts upstream of reactive oxygen species production. Plant Cell 14:3089–3099PubMedCrossRefGoogle Scholar
  44. 44.
    Yoshida R, Hobo T, Ichimura K et al (2002) ABA-activated SnRK2 protein kinase is required for dehydration stress signaling in Arabidopsis. Plant Cell Physiol 43:1473–1483PubMedCrossRefGoogle Scholar
  45. 45.
    Umezawa T, Yoshida R, Maruyama K, Yamaguchi-Shinozaki K, Shinozaki K (2004) SRK2C, a SNF1-related protein kinase 2, improves drought tolerance by controlling stress-responsive gene expression in Arabidopsis thaliana. Proc Natl Acad Sci USA 101:17306–17311PubMedCrossRefGoogle Scholar
  46. 46.
    Kobayashi Y, Murata M, Minami H et al (2005) Abscisic acid-activated SNRK2 protein kinases function in the gene-regulation pathway of ABA signal transduction by phosphorylating ABA response element-binding factors. Plant J 44:939–949PubMedCrossRefGoogle Scholar
  47. 47.
    Diédhiou CJ, Popova OV, Dietz K-J, Golldack D (2008) The SNF1-type serine-threonine protein kinase SAPK4 regulates stress-responsive gene expression in rice. BMC Plant Biol 8:49PubMedCrossRefGoogle Scholar
  48. 48.
    Saijo Y, Hata S, Kyozuka J, Shimamoto K, Izui K (2000) Over-expression of a single Ca2+-dependent protein kinase confers both cold and salt/drought tolerance on rice plants. Plant J 23:319–327PubMedCrossRefGoogle Scholar
  49. 49.
    Abbasi F, Onodera H, Toki S, Tanaka H, Komatsu S (2004) OsCDPK13, a calcium-dependent protein kinase gene from rice, is induced by cold and gibberellin in rice leaf sheath. Plant Mol Biol 55:541–552PubMedCrossRefGoogle Scholar
  50. 50.
    Gong D, Guo Y, Schumaker KS, Zhu J-K (2004) The SOS3 family of calcium sensors and SOS2 family of protein kinases in Arabidopsis. Plant Physiol 134:919–926PubMedCrossRefGoogle Scholar
  51. 51.
    Xiang Y, Huang Y, Xiong L (2007) Characterization of stress-responsive CIPK genes in rice for stress tolerance improvement. Plant Physiol 144:1416–1428PubMedCrossRefGoogle Scholar
  52. 52.
    Xiong L, Yang Y (2003) Disease resistance and abiotic stress tolerance in rice are inversely modulated by an abscisic acid-inducible mitogen-activated protein kinase. Plant Cell 15:745–759PubMedCrossRefGoogle Scholar
  53. 53.
    Chen THH, Murata N (2002) Enhancement of tolerance of abiotic stress by metabolic engineering of betaines and other compatible solutes. Curr Opin Plant Biol 5:250–257PubMedCrossRefGoogle Scholar
  54. 54.
    Igarashi Y, Yoshiba Y, Sanada Y, Yamaguchi-Shinozaki K, Wada K, Shinozaki K (1997) Characterization of the gene for Δ1-pyrroline-5-carboxylate synthetase and correlation between the expression of the gene and salt tolerance in Oryza sativa L. Plant Mol Biol 33:857–865PubMedCrossRefGoogle Scholar
  55. 55.
    Hien DT, Jacobs M, Angenon G et al (2003) Proline accumulation and Δ1-pyrroline-5-carboxylate synthetase gene properties in three rice cultivars differing in salinity and drought tolerance. Plant Sci 165:1059–1068CrossRefGoogle Scholar
  56. 56.
    Hur J, Jung K-H, Lee C-H, An G (2004) Stress-inducible OsP5CS2 gene is essential for salt and cold tolerance in rice. Plant Sci 167:417–426CrossRefGoogle Scholar
  57. 57.
    Zhu B, Su J, Chang M, Verma DPS, Fan Y-L, Wu R (1998) Overexpression of a Δ1-pyrroline-5-carboxylate synthetase gene and analysis of tolerance to water- and salt-stress in transgenic rice. Plant Sci 139:41–48CrossRefGoogle Scholar
  58. 58.
    Nanjo T, Kobayashi M, Yoshiba Y, Kakubari Y, Yamaguchi-Shinozaki K, Shinozaki K (1999) Antisense suppression of proline degradation improves tolerance to freezing and salinity in Arabidopsis thaliana. FEBS Lett 461:205–210PubMedCrossRefGoogle Scholar
  59. 59.
    Rhodes D, Hanson AD (1993) Quaternary ammonium and tertiary sulfonium compounds in higher plants. Annu Rev Plant Physiol Plant Mol Biol 44:357CrossRefGoogle Scholar
  60. 60.
    Chen THH, Murata N (2008) Glycinebetaine: an effective protectant against abiotic stress in plants. Trends Plant Sci 13:499–505PubMedCrossRefGoogle Scholar
  61. 61.
    Shirasawa K, Takabe T, Takabe T, Kishitani S (2006) Accumulation of glycinebetaine in rice plants that overexpress choline monooxygenase from spinach and evaluation of their tolerance to abiotic stress. Ann Bot 98:565–571PubMedCrossRefGoogle Scholar
  62. 62.
    Sakamoto A, Murata A, Murata N (1998) Metabolic engineering of rice leading to biosynthesis of glycinebetaine and tolerance to salt and cold. Plant Mol Biol 38:1011–1019PubMedCrossRefGoogle Scholar
  63. 63.
    Mohanty A, Kathuria H, Ferjani A et al (2002) Transgenics of an elite indica rice variety Pusa Basmati 1 harbouring the codA gene are highly tolerant to salt stress. Theor Appl Genet 106:51–57PubMedGoogle Scholar
  64. 64.
    Su J, Hirji R, Zhang L, He C, Selvaraj G, Wu R (2006) Evaluation of the stress-inducible production of choline oxidase in transgenic rice as a strategy for producing the stress-protectant glycine betaine. J Exp Bot 57:1129–1135PubMedCrossRefGoogle Scholar
  65. 65.
    Capell T, Bassie L, Christou P (2004) Modulation of the polyamine biosynthetic pathway in transgenic rice confers tolerance to drought stress. Proc Natl Acad Sci USA 101:9909–9914PubMedCrossRefGoogle Scholar
  66. 66.
    Roy M, Wu R (2002) Overexpression of S-adenosylmethionine decarboxylase gene in rice increases polyamine level and enhances sodium chloride-stress tolerance. Plant Sci 163:987–992CrossRefGoogle Scholar
  67. 67.
    Vijn I, Smeekens S (1999) Fructan: more than a reserve carbohydrate? Plant Physiol 120:351–360PubMedCrossRefGoogle Scholar
  68. 68.
    Ji X, Van den Ende W, Schroeven L et al (2007) The rice genome encodes two vacuolar invertases with fructan exohydrolase activity but lacks the related fructan biosynthesis genes of the Pooideae. New Phytol 173:50–62PubMedCrossRefGoogle Scholar
  69. 69.
    Kawakami A, Sato Y, Yoshida M (2008) Genetic engineering of rice capable of synthesizing fructans and enhancing chilling tolerance. J Exp Bot 59:793–802PubMedCrossRefGoogle Scholar
  70. 70.
    Paul MJ, Primavesi LF, Jhurreea D, Zhang Y (2008) Trehalose metabolism and signaling. Annu Rev Plant Biol 59:417–441PubMedCrossRefGoogle Scholar
  71. 71.
    Garg AK, Kim J-K, Owens TG et al (2002) Trehalose accumulation in rice plants confers high tolerance levels to different abiotic stresses. Proc Natl Acad Sci USA 99:15898–15903PubMedCrossRefGoogle Scholar
  72. 72.
    Pramanik MHR, Imai R (2005) Functional identification of a trehalose 6-phosphate phosphatase gene that is involved in transient induction of trehalose biosynthesis during chilling stress in rice. Plant Mol Biol 58:751–762PubMedCrossRefGoogle Scholar
  73. 73.
    Jang I-C, Oh S-J, Seo J-S et al (2003) Expression of a bifunctional fusion of the Escherichia coli genes for trehalose-6-phosphate synthase and trehalose-6-phosphate phosphatase in transgenic rice plants increases trehalose accumulation and abiotic stress tolerance without stunting growth. Plant Physiol 131:516–524PubMedCrossRefGoogle Scholar
  74. 74.
    Ge L-F, Chao D-Y, Shi M, Zhu M-Z, Gao J-P, Lin H-X (2008) Overexpression of the trehalose-6-phosphate phosphatase gene OsTPP1 confers stress tolerance in rice and results in the activation of stress responsive genes. Planta 228:191–201PubMedCrossRefGoogle Scholar
  75. 75.
    Taji T, Ohsumi C, Iuchi S et al (2002) Important roles of drought- and cold-inducible genes for galactinol synthase in stress tolerance in Arabidopsis thaliana. Plant J 29:417–426PubMedCrossRefGoogle Scholar
  76. 76.
    Nishida I, Murata N (1996) Chilling sensitivity in plants and cyanobacteria: the crucial contribution of membrane lipids. Annu Rev Plant Physiol Plant Mol Biol 47:541–568PubMedCrossRefGoogle Scholar
  77. 77.
    Zhu S-Q, Zhao H, Liang J-S, Ji B-H, Jiao D-M (2008) Relationships between phosphatidylglycerol molecular species of thylakoid membrane lipids and sensitivities to chilling-induced photoinhibition in rice. J Integr Plant Biol 50:194–202PubMedCrossRefGoogle Scholar
  78. 78.
    Murata N, Ishizaki-Nishizawa O, Higashi S, Hayashi H, Tasaka Y, Nishida I (1992) Genetically engineered alteration in the chilling sensitivity of plants. Nature 356:710–713CrossRefGoogle Scholar
  79. 79.
    Ariizumi T, Kishitani S, Inatsugi R, Nishida I, Murata N, Toriyama K (2002) An increase in unsaturation of fatty acids in phosphatidylglycerol from leaves improves the rates of photosynthesis and growth at low temperatures in transgenic rice seedlings. Plant Cell Physiol 43:751–758PubMedCrossRefGoogle Scholar
  80. 80.
    Yokoi S, Higashi S-I, Kishitani S, Murata N, Toriyama K (1998) Introduction of the cDNA for shape Arabidopsis glycerol-3-phosphate acyltransferase (GPAT) confers unsaturation of fatty acids and chilling tolerance of photosynthesis on rice. Mol Breed 4:269–275CrossRefGoogle Scholar
  81. 81.
    Upchurch RG (2008) Fatty acid unsaturation, mobilization, and regulation in the response of plants to stress. Biotechnol Lett 30:967–977PubMedCrossRefGoogle Scholar
  82. 82.
    Matsuda O, Iba K (2005) Trienoic fatty acids and stress responses in higher plants. Plant Biotechnol 22:423–430CrossRefGoogle Scholar
  83. 83.
    Battaglia M, Olvera-Carrillo Y, Garciarrubio A, Campos F, Covarrubias AA (2008) The enigmatic LEA proteins and other hydrophilins. Plant Physiol 148:6–24PubMedCrossRefGoogle Scholar
  84. 84.
    Hundertmark M, Hincha DK (2008) LEA (late embryogenesis abundant) proteins and their encoding genes in Arabidopsis thaliana. BMC Genomics 9:118PubMedCrossRefGoogle Scholar
  85. 85.
    Moons A, Bauw G, Prinsen E, Van Montagu M, Van Der Straeten D (1995) Molecular and physiological responses to abscisic acid and salts in roots of salt-sensitive and salt-tolerant indica rice varieties. Plant Physiol 107:177–186PubMedCrossRefGoogle Scholar
  86. 86.
    Aguan K, Sugawara K, Suzuki N, Kusano T (1991) Isolation of genes for low-temperature-induced proteins in rice by a simple subtractive method. Plant Cell Physiol 32:1285–1289Google Scholar
  87. 87.
    Xu D, Duan X, Wang B, Hong B, Ho T-HD, Wu R (1996) Expression of a late embryogenesis abundant protein gene, HVA1, from barley confers tolerance to water deficit and salt stress in transgenic rice. Plant Physiol 110:249–257PubMedGoogle Scholar
  88. 88.
    Rohila JS, Jain RK, Wu R (2002) Genetic improvement of basmati rice for salt and drought tolerance by regulated expression of a barley Hva1 cDNA. Plant Sci 163:525–532CrossRefGoogle Scholar
  89. 89.
    Xiao B, Huang Y, Tang N, Xiong L (2007) Over-expression of a LEA gene in rice improves drought resistance under the field conditions. Theor Appl Genet 115:35–46PubMedCrossRefGoogle Scholar
  90. 90.
    Kotak S, Larkindale J, Lee U, von Koskull-Döing P, Vierling E, Scharf K-D (2007) Complexity of the heat stress response in plants. Curr Opin Plant Biol 10:310–316PubMedCrossRefGoogle Scholar
  91. 91.
    Katiyar-Agarwal S, Agarwal M, Grover A (2003) Heat-tolerant basmati rice engineered by over-expression of hsp101. Plant Mol Biol 51:677–686PubMedCrossRefGoogle Scholar
  92. 92.
    Sato Y, Yokoya S (2008) Enhanced tolerance to drought stress in transgenic rice plants overexpressing a small heat-shock protein, sHSP17.7. Plant Cell Rep 27:329–334PubMedCrossRefGoogle Scholar
  93. 93.
    Ren Z-H, Gao J-P, Li L-G et al (2005) A rice quantitative trait locus for salt tolerance encodes a sodium transporter. Nat Genet 37:1141–1146PubMedCrossRefGoogle Scholar
  94. 94.
    Shi H, Quintero FJ, Pardo JM, Zhu J-K (2002) The putative plasma membrane Na+/H+ antiporter SOS1 controls long-distance Na+ transport in plants. Plant Cell 14:465–477PubMedCrossRefGoogle Scholar
  95. 95.
    Martínez-Atienza J, Jiang X, Garciadeblas B et al (2007) Conservation of the salt overly sensitive pathway in rice. Plant Physiol 143:1001–1012PubMedCrossRefGoogle Scholar
  96. 96.
    Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681PubMedCrossRefGoogle Scholar
  97. 97.
    Apse MP, Aharon GS, Snedden WA, Blumwald E (1999) Salt tolerance conferred by overexpression of a vacuolar Na+/H+ antiport in Arabidopsis. Science 285:1256–1258PubMedCrossRefGoogle Scholar
  98. 98.
    Apse MP, Sottosanto JB, Blumwald E (2003) Vacuolar cation/H+ exchange, ion homeostasis, and leaf development are altered in a T-DNA insertional mutant of AtNHX1, the Arabidopsis vacuolar Na+/H+ antiporter. Plant J 36:229–239PubMedCrossRefGoogle Scholar
  99. 99.
    Ohta M, Hayashi Y, Nakashima A et al (2002) Introduction of a Na+/H+ antiporter gene from Atriplex gmelini confers salt tolerance to rice. FEBS Lett 532:279–282PubMedCrossRefGoogle Scholar
  100. 100.
    Fukuda A, Nakamura A, Tagiri A et al (2004) Function, intracellular localization and the importance in salt tolerance of a vacuolar Na+/H+ antiporter from rice. Plant Cell Physiol 45:146–159PubMedCrossRefGoogle Scholar
  101. 101.
    Chen H, An R, Tang J-H et al (2007) Over-expression of a vacuolar Na+/H+ antiporter gene improves salt tolerance in an upland rice. Mol Breed 19:215–225CrossRefGoogle Scholar

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© Springer Science+Business Media, LLC 2013

Authors and Affiliations

  1. 1.Laboratory of Plant Molecular Physiology, Graduate School of Agricultural and Life SciencesUniversity of TokyoTokyoJapan

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